water Article How Did the Late 1980s Climate Regime Shift Affect Temperature-Sensitive Fish Population Dynamics: Case Study of Vendace (Coregonus albula) in a Large North-Temperate Lake Külli Kangur * , Kai Ginter, Andu Kangur y, Peeter Kangur and Tõnu Möls y Centre for Limnology, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, 61117 Rannu, Estonia; [email protected] (K.G.); [email protected] (P.K.) * Correspondence: [email protected]; Tel.: +372-5246085 The two co-authors have passed away and however their great contribution to the development of this y manuscript needs to be acknowledged as co-authors. Received: 30 July 2020; Accepted: 23 September 2020; Published: 26 September 2020 Abstract: The population dynamics of fish in northern lakes is strongly influenced by climatic factors. In this study, we investigated whether there is a link between the late 1980s climate regime shift in Europe and the collapse of vendace (Coregonus albula) population at the same time in Lake Peipsi. Until the end of the 1980s, vendace was very abundant in the lake, but then its catches sharply declined. This decline inspired investigations into the extreme weather events preceding the vendace collapse using data on daily water temperatures and ice phenology together with commercial fishery statistics since 1931 and test catch data since 1986. We identified using advanced statistical methods that the hot summer of 1988, which was accompanied by a severe cyanobacterial bloom and extensive fish kill, and the subsequent non-permanent ice cover and early ice-offs in 1989 and 1990 in Lake Peipsi were the main reasons for the disappearance of vendace from catches in 1991. Moreover, a negative correlation appeared between catches of the predatory pikeperch (Sander lucioperca) and vendace. Predation pressure as well as fish habitat degradation caused by lake eutrophication may contribute to the instability of the vendace population too. Our study showed that extreme weather events such as heat waves in summer and non-permanent ice-cover in winter in consecutive years may have long-lasting harmful effects on the population abundance of cool-water fish species such as vendace whose eggs usually develop under an ice cover in north-temperate lakes. Keywords: climate regime shift; extreme weather events; phenology of lake ice; population dynamics of vendace; predator–prey interactions 1. Introduction Declines and collapses of fish populations have frequently been attributed to local human interventions, including over-exploitation of fisheries [1–4] and habitat loss due to pollution [5]. Additionally, predator–prey interactions [6], parasite infections [7] and climate can trigger the reduction of fish species. Although natural factors are not frequently reported to cause the collapse of fish populations [8–10], climate may influence fish populations through a variety of direct and indirect processes [11,12]. The impact of abrupt climatic shifts on lake ecosystems will likely differ from the effects of long-term gradual warming [13]. Decline and collapse of fish populations at different geographical scales have been widely reported in recent decades [2,9,14]. In Europe’s fourth largest lake, Lake Peipsi (Estonia/Russia), vendace (Coregonus albula) was the dominant fish species and the main target of commercial fishery until the end Water 2020, 12, 2694; doi:10.3390/w12102694 www.mdpi.com/journal/water Water 2020, 12, 2694 2 of 16 of the 1980s; however, it dramatically declined thereafter. Similarly, vendace abundance has declined in Finland (e.g., Lake Pyhäjärvi and Lake Puulavesi [15–17]), Sweden (Lake Mälaren [18]) and the United Kingdom (Lake Bassenthwaite; [19,20]). However, in the northern distribution area of vendace, such as Finland, the stock has recovered and fish are abundant [21]. Vendace is a typical lacustrine coregonid occurring principally in northern European freshwater ecosystems [22,23]. It is a small-bodied shoaling pelagic fish that prefers cold water (e.g., [18,24–26]). Adult vendace avoid areas where the temperature exceeds 18–19 ◦C or the concentration of oxygen 1 is less than 2 mg L− [19,23,27,28]. Vendace has a cold-water thermal window characterized by a metabolic optimum approximately 7–9 ◦C[29–31]. According to Potapova [32], vendace feeds most intensively at 15–16 ◦C, and the intensity of its feeding drops when the temperature rises to 18–20 ◦C. In Estonian waters, vendace spawns in November to December at a temperature of 0.2–3 ◦C and hatching takes place in the middle of April [33]. In Lake Peipsi, vendace attains sexual maturity at the age of two years and has a typical lifespan of only 3–5 years [34]. Due to its preference for cold water and its peculiar life history, such as autumn spawning, short lifespan and early reproduction [26,35,36], vendace populations are very vulnerable to habitat changes and have substantially fluctuating abundances [16]. The literature reports that high water temperatures [29,30], low oxygen levels [19,23,28] and variability of ice conditions [18,37] may have negative effects on vendace populations. Additionally, co-occurring stressors, for instance long-term eutrophication [38], fishing pressure [36] and predator–prey interactions [39–42], may deepen the effect of climate change on the year-class strength and population dynamics of vendace [14]. Although many complex interactions may cause reduction in the abundance of species, the potential effects of such interacting components of the global climate change on biotic communities remain poorly elucidated [11,43–45]. Moreover, the effects of extreme weather events on ecosystems are much less understood than the effects of longer-term changes in average environmental conditions [46], and there is a pressing need to extend current understanding of abrupt changes in ecological systems as climate warming accelerates [47]. Therefore, analyzing the long-term population dynamics of vendace and coupling the results with data on climatic factors, water quality and fish community features in Lake Peipsi could contribute new knowledge about the factors affecting the decline and collapse of fish populations in the north temperate region. In the present study, we used vendace as a biological model to study the relationship between climate regime shift and population collapse. Other sensitive cool-water fish declining in the lake (e.g., burbot Lota lota and Peipsi whitefish Coregonus lavaretus maraenoides) are longer-lived than vendace and likely to respond more slowly to environmental change. We used a nearly nine-decade dataset on vendace commercial catches and lake surface water temperature (LSWT) parameters with the aim of clarifying the relationships between extreme weather events related to the late 1980s regional climate regime shift [48,49] and vendace catch dynamics in Lake Peipsi. The specific focus of our study was to identify the environmental variables most related to the collapse of the vendace population in Lake Peipsi by the turn of the 1980/1990 decade. We hypothesized that the drastic reduction of the vendace population and catches was linked to the cumulative effects of warm water temperature extremes and fish kills during heat waves in summer and the extreme ice conditions in winter during the years before the disappearance of vendace from the commercial fish catches. We investigated the differences in environmental conditions between the three consecutive years immediately preceding the collapse and the “ordinary” years since the 1930s. Additionally, the potential influences of the flourishing pikeperch (Sander lucioperca) population, the high fishing pressure and continued cultural eutrophication of Lake Peipsi [50,51] on the vendace stock were discussed. Water 2020, 12, x FOR PEER REVIEW 3 of 16 investigated the differences in environmental conditions between the three consecutive years immediately preceding the collapse and the “ordinary” years since the 1930s. Additionally, the potential influences of the flourishing pikeperch (Sander lucioperca) population, the high fishing pressure and continued cultural eutrophication of Lake Peipsi [50,51] on the vendace stock were discussed. Water 2020, 12, 2694 3 of 16 2. Material and Methods 2. Material and Methods 2.1. Study Area 2.1.Lake Study Peipsi Area (57°51′–59°01′ N; 26°57′–28°10′ E) is the fourth largest lake in Europe, located south of the Gulf of Finland on the border of Estonia and Russia (Figure 1). Peipsi is a polymictic and Lake Peipsi (57◦510–59◦010 N; 26◦570–28◦100 E) is the fourth largest lake in Europe, located south shallowof the Gulf lowland of Finland lake (Table on the 1) border with ofa surface Estonia area and Russiaof 3555 (Figure km2 and1). a Peipsi mean iswat a polymicticer level of and30 m shallow above sealowland level. lakeIn fact, (Table Lake1) Peipsi, with a surfacewhich is area elongated of 3555 more km 2 andthan a 150 mean km water in the level north of– 30south m above direction, sea level. is a lakeIn fact, system, Lake consisting Peipsi, which of three is elongated limnologically more than different 150 km parts: in the Lake north–south Peipsi s.s. direction, (mean and is a lakemaximum system, depthconsisting 8.3 and of three12.9 m, limnologically respectively), di ffLakeerent Lämmijärv parts: Lake (2.5 Peipsi and s.s. 15.3 (mean m) and and Lake maximum Pihkva depth (3.8 and 8.3 and5.3 m).12.9 Lake m, respectively), Peipsi’s water Lake level Lämmijärv is not (2.5 regulated; and 15.3 m)however, and Lake natural Pihkva water (3.8 and level 5.3 m).fluctuations Lake Peipsi’s are considerable,water level is with not regulated; an overall however, range of natural3.04 m waterover the level last fluctuations 80 years and are a considerable, mean annual with range an of overall 1.15 mrange [52]. of Situated 3.04 m overin the the north last 80 temperate years and region, a mean in annual the transition range of 1.15zone m between [52].